Publications from The Sainsbury Laboratory
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PLoS One: Comprehensive Transcriptome Analysis Unravels the Existence of Crucial Genes Regulating Primary Metabolism during Adventitious Root Formation in Petunia hybrida (2014)

PLoS One: Comprehensive Transcriptome Analysis Unravels the Existence of Crucial Genes Regulating Primary Metabolism during Adventitious Root Formation in Petunia hybrida (2014) | Publications from The Sainsbury Laboratory | Scoop.it
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To identify specific genes determining the initiation and formation of adventitious roots (AR), a microarray-based transcriptome analysis in the stem base of the cuttings of Petunia hybrida (line W115) was conducted. A microarray carrying 24,816 unique, non-redundant annotated sequences was hybridized to probes derived from different stages of AR formation. After exclusion of wound-responsive and root-regulated genes, 1,354 of them were identified which were significantly and specifically induced during various phases of AR formation. Based on a recent physiological model distinguishing three metabolic phases in AR formation, the present paper focuses on the response of genes related to particular metabolic pathways. Key genes involved in primary carbohydrate metabolism such as those mediating apoplastic sucrose unloading were induced at the early sink establishment phase of AR formation. Transcriptome changes also pointed to a possible role of trehalose metabolism and SnRK1 (sucrose non-fermenting 1- related protein kinase) in sugar sensing during this early step of AR formation. Symplastic sucrose unloading and nucleotide biosynthesis were the major processes induced during the later recovery and maintenance phases. Moreover, transcripts involved in peroxisomal beta-oxidation were up-regulated during different phases of AR formation. In addition to metabolic pathways, the analysis revealed the activation of cell division at the two later phases and in particular the induction of G1-specific genes in the maintenance phase. Furthermore, results point towards a specific demand for certain mineral nutrients starting in the recovery phase.

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bioRxiv: An Oomycete Effector Protein Induces Shade Avoidance In Arabidopsis And Attenuates Salicylate Signaling By Binding To Host Proteins Of The RADICAL-INDUCED CELL DEATH1 Family (2017)

bioRxiv: An Oomycete Effector Protein Induces Shade Avoidance In Arabidopsis And Attenuates Salicylate Signaling By Binding To Host Proteins Of The RADICAL-INDUCED CELL DEATH1 Family (2017) | Publications from The Sainsbury Laboratory | Scoop.it
bioRxiv - the preprint server for biology, operated by Cold Spring Harbor Laboratory, a research and educational institution
The Sainsbury Lab's insight:
The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. During infection, Hpa like other biotrophic pathogens, suppresses activation of plant innate immunity by translocating effector proteins into host cells. Some of these effectors localize to the host cell nucleus where they may manipulate transcriptional reprogramming of plant defense genes. Here we report that the nuclear-localized Hpa effector HaRxL106, when expressed in Arabidopsis, induces shade avoidance and attenuates the transcriptional response to the defense signaling molecule salicylic acid. HaRxL106 interacts with RADICAL-INDUCED CELL DEATH1 (RCD1) and loss of RCD1 function renders Arabidopsis resilient against HaRxL106-mediated suppression of immunity. To further characterize the molecular functions of RCD1 we solved a crystal structure of the RCD1 Poly-(ADP-ribose)-Polymerase (PARP) domain and, based on non-conservation of amino acids constituting the active site of canonical PARPs, conclude that RCD1 has no PARP activity. We report that RCD1-type proteins are phosphorylated and identified histone-modifying Mut9-like kinases (MLKs) as RCD1-interacting proteins. A mlk1,3,4 triple mutant exhibits stronger SA-induced defense marker gene expression compared to wild-type plants. Our data suggest that HaRxL106 suppresses Arabidopsis innate immunity by manipulating the function(s) of RCD1 in the host cell nucleus and point towards a role of RCD1 as a transcriptional co-regulator that integrates signals from light and pathogen sensors.
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Curr Opin Plant Biol: NLR diversity, helpers and integrated domains: making sense of the NLR IDentity (2017)

Curr Opin Plant Biol: NLR diversity, helpers and integrated domains: making sense of the NLR IDentity (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
Plant innate immunity relies on genetically predetermined repertoires of immune receptors to detect pathogens and trigger an effective immune response. A large proportion of these receptors are from the Nucletoide Binding Leucine Rich Repeat (NLR) gene family. As plants live longer than most pathogens, maintaining diversity of NLRs and deploying efficient ‘pathogen traps’ is necessary to withstand the evolutionary battle. In this review, we summarize the sources of diversity in NLR plant immune receptors giving an overview of genomic, regulatory as well as functional studies, including the latest concepts of NLR helpers and NLRs with integrated domains.
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PLoS Pathogens: Protein-protein interactions in the RPS4/RRS1 immune receptor complex (2017)

PLoS Pathogens: Protein-protein interactions in the RPS4/RRS1 immune receptor complex (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Plant NLR (Nucleotide-binding domain and Leucine-rich Repeat) immune receptor proteins are encoded by Resistance (R) genes and confer specific resistance to pathogen races that carry the corresponding recognized effectors. Some NLR proteins function in pairs, forming receptor complexes for the perception of specific effectors. We show here that the Arabidopsis RPS4 and RRS1 NLR proteins are both required to make an authentic immune complex. Over-expression of RPS4 in tobacco or in Arabidopsis results in constitutive defense activation; this phenotype is suppressed in the presence of RRS1. RRS1 protein co-immunoprecipitates (co-IPs) with itself in the presence or absence of RPS4, but in contrast, RPS4 does not associate with itself in the absence of RRS1. In the presence of RRS1, RPS4 associates with defense signaling regulator EDS1 solely in the nucleus, in contrast to the extra-nuclear location found in the absence of RRS1. The AvrRps4 effector does not disrupt RPS4-EDS1 association in the presence of RRS1. In the absence of RRS1, AvrRps4 interacts with EDS1, forming nucleocytoplasmic aggregates, the formation of which is disturbed by the co-expression of PAD4 but not by SAG101. These data indicate that the study of an immune receptor protein complex in the absence of all components can result in misleading inferences, and reveals an NLR complex that dynamically interacts with the immune regulators EDS1/PAD4 or EDS1/SAG101, and with effectors, during the process by which effector recognition is converted to defense activation.
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Genome Res: An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations (2017)

Genome Res: An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations (2017) | Publications from The Sainsbury Laboratory | Scoop.it
An international, peer-reviewed genome sciences journal featuring outstanding original research that offers novel insights into the biology of all organisms
The Sainsbury Lab's insight:
Advances in genome sequencing and assembly technologies are generating many high-quality genome sequences, but assemblies of large, repeat-rich polyploid genomes, such as that of bread wheat, remain fragmented and incomplete. We have generated a new wheat whole-genome shotgun sequence assembly using a combination of optimized data types and an assembly algorithm designed to deal with large and complex genomes. The new assembly represents >78% of the genome with a scaffold N50 of 88.8 kb that has a high fidelity to the input data. Our new annotation combines strand-specific Illumina RNA-seq and Pacific Biosciences (PacBio) full-length cDNAs to identify 104,091 high-confidence protein-coding genes and 10,156 noncoding RNA genes. We confirmed three known and identified one novel genome rearrangements. Our approach enables the rapid and scalable assembly of wheat genomes, the identification of structural variants, and the definition of complete gene models, all powerful resources for trait analysis and breeding of this key global crop.
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MPMI: Foundational and translational research opportunities to improve plant health (2017)

MPMI: Foundational and translational research opportunities to improve plant health (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
This whitepaper reports the deliberations of a workshop focused on biotic challenges to plant health held in Washington, D.C. in September 2016. Ensuring health of food plants is critical to maintaining the quality and productivity of crops and for sustenance of the rapidly growing human population. There is a close linkage between food security and societal stability; however, global food security is threatened by the vulnerability of our agricultural systems to numerous pests, pathogens, weeds, and environmental stresses. These threats are aggravated by climate change, the globalization of agriculture, and an over-reliance on non-sustainable inputs. New analytical and computational technologies are providing unprecedented resolution at a variety of molecular, cellular, organismal, and population scales for crop plants as well as pathogens, pests, beneficial microbes, and weeds. It is now possible to both characterize useful or deleterious variation as well as precisely manipulate it. Data-driven, informed decisions based on knowledge of the variation of biotic challenges and of natural and synthetic variation in crop plants will enable deployment of durable interventions throughout the world. These should be integral, dynamic components of agricultural strategies for sustainable agriculture.

Specific findings:
● Genetic improvement of crops is the most reliable, least expensive management strategy when suitable genetic variation is available. Nonetheless, some interventions have not proved durable due to the evolution and global dispersal of virulent pathogens and pests as well as herbicide-resistant weeds.
● Additional strategies are becoming essential as multiple fungicides, nematicides, and herbicides become ineffective due to the evolution of resistance and/or are phased out due to registration withdrawals.
● Strategies are needed that maximize the evolutionary hurdles for pathogens, pests, and weeds to overcome control measures. Interventions need to evolve as fast as the biotic challenges. Moreover, deployments of interventions must be driven by knowledge of the evolutionary capacity of the biotic challenge.
● Considerable knowledge exists but more research into the mechanisms of plant immunity and other forms of resistance is needed as the foundation for translational applications.
● Several new technologies are increasing foundational knowledge and providing numerous opportunities for generating crops with durable resistance to pests and diseases as well as control of weeds and reduction of the environmental impact of agriculture.
● There are multiple strategies for counteracting biotic challenges involving canonical and non-canonical disease resistance genes, genes encoding susceptibility factors, small RNAs, or immunomodulators. Simultaneous deployment of disease resistance strategies with different modes of action, as well as the judicious use of fungicides, will enhance durability of control measures.
● Pathogen effectors provide tools for discovering resistance genes and susceptibility factors as well as for dissecting/manipulating plant biology and breeding plants for durable disease resistance.
● There are several, as yet little exploited, opportunities for leveraging beneficial interactions among plants, microbes, insects and other organisms in the phytobiome to enhance plant health and productivity as well as breeding plants to promote beneficial phytobiome communities.
● Global monitoring of plant health is feasible and desirable in order to anticipate and counter threats.
● Climate change increases the need for continual global monitoring of pathogens, pests, and weeds and adjusting of control strategies.
● There are numerous current and future opportunities for knowledge exchange and partnerships between developed and developing countries to foster improved local and global food security.
● Both genetically modified (GM) and non-GM strategies are needed to maximize plant health and food security.
● Significant, sustained financial support is required if the beneficial impacts of foundational and translational research on global food security are to be realized.

The needs, opportunities, approaches, and deliverables for addressing biotic challenges to plant health are detailed in Table 1. These can be broadly classified as assessing variation, characterizing it in detail at a variety of scales, and deploying beneficial interventions. Immediate investments in global monitoring of pathogens/pests and in situ and ex-situ determination of what natural variation exists in crop plants for countering challenges and threats should be a high priority. Detailed investigations of the molecular basis of the various types of plant resistance and of the basis of pathogen/pest virulence are critical for providing the foundation for novel intervention strategies; these will be facilitated by development of high resolution structural and functional analytical techniques. Optimization of protocols for delivery of reagents for allele replacement and gene insertions into diverse major and minor crop plants should be a high priority. Monitoring and deployment should be a global endeavor involving multinational partnerships and knowledge exchanges in order to ensure that interventions are locally relevant and globally durable.
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Sci Rep: Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion (2017)

Sci Rep: Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion (2017) | Publications from The Sainsbury Laboratory | Scoop.it
Article
The Sainsbury Lab's insight:
Genome editing has emerged as a technology with a potential to revolutionize plant breeding. In this study, we report on generating, in less than ten months, Tomelo, a non-transgenic tomato variety resistant to the powdery mildew fungal pathogen using the CRISPR/Cas9 technology. We used whole-genome sequencing to show that Tomelo does not carry any foreign DNA sequences but only carries a deletion that is indistinguishable from naturally occurring mutations. We also present evidence for CRISPR/Cas9 being a highly precise tool, as we did not detect off-target mutations in Tomelo. Using our pipeline, mutations can be readily introduced into elite or locally adapted tomato varieties in less than a year with relatively minimal effort and investment.
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Nature: Plant signalling in symbiosis and immunity (2017)

Nature: Plant signalling in symbiosis and immunity (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
Plants encounter a myriad of microorganisms, particularly at the root–soil interface, that can invade with detrimental or beneficial outcomes. Prevalent beneficial associations between plants and microorganisms include those that promote plant growth by facilitating the acquisition of limiting nutrients such as nitrogen and phosphorus. But while promoting such symbiotic relationships, plants must restrict the formation of pathogenic associations. Achieving this balance requires the perception of potential invading microorganisms through the signals that they produce, followed by the activation of either symbiotic responses that promote microbial colonization or immune responses that limit it.
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Theor Appl Genet: Discovery and characterization of two new stem rust resistance genes in Aegilops sharonensis (2017)

Theor Appl Genet: Discovery and characterization of two new stem rust resistance genes in Aegilops sharonensis (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Stem rust is one of the most important diseases of wheat in the world. When single stem rust resistance (Sr) genes are deployed in wheat, they are often rapidly overcome by the pathogen. To this end, we initiated a search for novel sources of resistance in diverse wheat relatives and identified the wild goatgrass species Aegilops sharonesis (Sharon goatgrass) as a rich reservoir of resistance to wheat stem rust. The objectives of this study were to discover and map novel Sr genes in Ae. sharonensis and to explore the possibility of identifying new Sr genes by genome-wide association study (GWAS). We developed two biparental populations between resistant and susceptible accessions of Ae. sharonensis and performed QTL and linkage analysis. In an F6 recombinant inbred line and an F2 population, two genes were identified that mapped to the short arm of chromosome 1Ssh, designated as Sr-1644-1Sh, and the long arm of chromosome 5Ssh, designated as Sr-1644-5Sh. The gene Sr-1644-1Sh confers a high level of resistance to race TTKSK (a member of the Ug99 race group), while the gene Sr-1644-5Sh conditions strong resistance to TRTTF, another widely virulent race found in Yemen. Additionally, GWAS was conducted on 125 diverse Ae. sharonensis accessions for stem rust resistance. The gene Sr-1644-1Sh was detected by GWAS, while Sr-1644-5Sh was not detected, indicating that the effectiveness of GWAS might be affected by marker density, population structure, low allele frequency and other factors.
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eLife: Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains (2017)

eLife: Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Cell surface receptors govern a multitude of signalling pathways in multicellular organisms. In plants, prominent examples are the receptor kinases FLS2 and BRI1, which activate immunity and steroid-mediated growth, respectively. Intriguingly, despite inducing distinct signalling outputs, both receptors employ common downstream signalling components, which exist in plasma membrane (PM)-localised protein complexes. An important question is thus how these receptor complexes maintain signalling specificity. Live-cell imaging revealed that FLS2 and BRI1 form PM nanoclusters. Using single-particle tracking we could discriminate both cluster populations and we observed spatiotemporal separation between immune and growth signalling platforms. This finding was confirmed by visualising FLS2 and BRI1 within distinct PM nanodomains marked by specific remorin proteins and differential co-localisation with the cytoskeleton. Our results thus suggest that signalling specificity between these pathways may be explained by the spatial separation of FLS2 and BRI1 with their associated signalling components within dedicated PM nanodomains.
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Plant Physiol: Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses (2017)

Plant Physiol: Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
The plant cell wall, often the site of initial encounters between plants and their microbial pathogens, is composed of a complex mixture of cellulose, hemicellulose and pectin polysaccharides, as well as proteins. The concept of damage-associated molecular patterns (DAMPs) was proposed to describe plant elicitors like oligogalacturonides (OGs), which can be derived by the breakdown of the pectin homogalacturon by pectinases. OGs act via many of the same signaling steps as pathogen- or microbe-associated molecular patterns (PAMPs) to elicit defenses and provide protection against pathogens. Given both the complexity of the plant cell wall and the fact that many pathogens secrete a wide range of cell wall degrading enzymes, we reasoned that the breakdown products of other cell wall polymers may be similarly biological active as elicitors and may help to reinforce the perception of danger by plant cells. Our results indicate that oligomers derived from cellulose are perceived as signal molecules in Arabidopsis, triggering a signaling cascade that shares some similarities to responses to well-known elicitors such as chito-oligomers and OGs. However, in contrast to other known P/DAMPs, cellobiose stimulates neither detectable ROS production nor callose deposition. Confirming our idea that both PAMPs and DAMPs are likely to co-occur at infection sites, co-treatments of cellobiose with flg22 or chito-oligomers led to synergistic increases in gene expression. Thus, the perception of cellulose-derived oligomers may participate in cell wall integrity surveillance, and represents an additional layer of signaling following plant cell wall breakdown during cell wall remodeling or pathogen attack.
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Genetics: Genomic Rearrangements in Arabidopsis Considered as Quantitative Traits (2017)

Genetics: Genomic Rearrangements in Arabidopsis Considered as Quantitative Traits (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
To understand the population genetics of structural variants and their effects on phenotypes, we developed an approach to mapping structural variants that segregate in a population sequenced at low coverage. We avoid calling structural variants directly. Instead, the evidence for a potential structural variant at a locus is indicated by variation in the counts of short-reads that map anomalously to that locus. These structural variant traits are treated as quantitative traits and mapped genetically, analogously to a gene expression study. Association between a structural variant trait at one locus and genotypes at a distant locus indicate the origin and target of a transposition. Using ultra-low-coverage (0.3x) population sequence data from 488 recombinant inbred Arabidopsis thaliana genomes, we identified 6,502 segregating structural variants. Remarkably, 25% of these were transpositions. Whilst many structural variants cannot be delineated precisely, we validated 83% of 44 predicted transposition breakpoints by polymerase chain reaction. We show that specific structural variants may be causative for quantitative trait loci for germination and resistance to infection by the fungus Albugo laibachii, isolate Nc14. Further we show that the phenotypic heritability attributable to read-mapping anomalies differs from, and in the case of time to germination and bolting, exceeds that due to standard genetic variation. Genes within structural variants are also more likely to be silenced or dysregulated. This approach complements the prevalent strategy of structural variant discovery in fewer individuals sequenced at high coverage. It is generally applicable to large populations sequenced at low-coverage, and is particularly suited to mapping transpositions.
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bioRxiv: Host autophagosomes are diverted to a plant-pathogen interface (2017)

bioRxiv: Host autophagosomes are diverted to a plant-pathogen interface (2017) | Publications from The Sainsbury Laboratory | Scoop.it

Filamentous plant pathogens and symbionts invade their host cells but remain enveloped by host-derived membranes. The mechanisms underlying the biogenesis and functions of these host-microbe interfaces are poorly understood. Recently, we showed that PexRD54, an effector from the Irish potato famine pathogen Phytophthora infestans, binds host protein ATG8CL to stimulate autophagosome formation and deplete the selective autophagy receptor Joka2 from ATG8CL complexes. Here, we show that during P. infestans infection, ATG8CL autophagosomes are diverted to the pathogen interface. Our findings are consistent with the view that the pathogen coopts host selective autophagy for its own benefit.


Via Kamoun Lab @ TSL
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Dev Cell: Mis-placed Congeniality: When Pathogens Ask Their Plant Hosts for Another Drink (2017)

Dev Cell: Mis-placed Congeniality: When Pathogens Ask Their Plant Hosts for Another Drink (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
Plants control nutrient availability in intercellular spaces (the apoplast) via transporters, channels, and vesicular transport. Recent papers in Science and Nature from two groups have highlighted how plants control sugar to restrict bacterial growth (Yamada et al., 2016) and how increased water availability enhances pathogenesis (Xin et al., 2016).
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PNAS: Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity (2017)

PNAS: Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity (2017) | Publications from The Sainsbury Laboratory | Scoop.it
National Academy of Sciences
The Sainsbury Lab's insight:
Plants detect and respond to pathogen invasion with membrane-localized pattern recognition receptors (PRRs), which recognize pathogen-associated molecular patterns (PAMPs) and activate downstream immune responses. Here we report that Arabidopsis thaliana LORELEI-LIKE GPI-ANCHORED PROTEIN 1 (LLG1), a coreceptor of the receptor-like kinase FERONIA, regulates PRR signaling. In a forward genetic screen for suppressors of enhanced disease resistance 1 (edr1), we identified the point mutation llg1-3, which suppresses edr1 disease resistance but does not affect plant growth and development. The llg1 mutants show enhanced susceptibility to various virulent pathogens, indicating that LLG1 has an important role in plant immunity. LLG1 constitutively associates with the PAMP receptor FLAGELLIN SENSING 2 (FLS2) and the elongation factor-Tu receptor, and forms a complex with BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED RECEPTOR KINASE 1 in a ligand-dependent manner, indicating that LLG1 functions as a key component of PAMP-recognition immune complexes. Moreover, LLG1 contributes to accumulation and ligand-induced degradation of FLS2, and is required for downstream innate immunity responses, including ligand-induced phosphorylation of BOTRYTIS-INDUCED KINASE 1 and production of reactive oxygen species. Taken together, our findings reveal that LLG1 associates with PAMP receptors and modulates their function to regulate disease responses. As LLG1 functions as a coreceptor of FERONIA and plays central roles in plant growth and development, our findings indicate that LLG1 participates in separate pathways, and may suggest a potential connection between development and innate immunity in plants.
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BMC Biol: Can a biologist fix a smartphone?—Just hack it! (2017)

BMC Biol: Can a biologist fix a smartphone?—Just hack it! (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Biological systems integrate multiscale processes and networks and are, therefore, viewed as difficult to dissect. However, because of the clear-cut separation between the software code (the information encoded in the genome sequence) and hardware (organism), genome editors can operate as software engineers to hack biological systems without any particularly deep understanding of the complexity of the systems.

This article was inspired by the influential and entertaining essay by Yuri Lazebnik who argued that there are fundamental flaws in how biologists approach problems [1]. Lazebnik proposed that the complexity of biological systems calls for a systems approach to the study of living systems using a radio as a colourful metaphor to illustrate his points [1]. He postulated that, conceptually, a radio functions similarly to a biological system by converting a signal from one form into another using a signal transduction pathway [1]. Here I argue that Lazebnik’s thesis is limited by two fundamental principles of biology. First, the clear-cut separation between the software code—the operating information for living systems as written in the genome sequence—and hardware, or the organism itself [2, 3]. Second, biological systems are not optimally designed but are shaped by historicity—the historical constraints that are integral to their evolution [4]. This limits the extent to which principles of design and engineering can be useful in understanding and manipulating the structures and functions of living organisms. In contrast, modern day biologists are starting to operate as software engineers to hack biological systems and write apps despite a somewhat superficial understanding of the underlying complexity of these systems.
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PLoS Genetics: The highly buffered Arabidopsis immune signaling network conceals the functions of its components (2017)

PLoS Genetics: The highly buffered Arabidopsis immune signaling network conceals the functions of its components (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Plant immunity protects plants from numerous potentially pathogenic microbes. The biological network that controls plant inducible immunity must function effectively even when network components are targeted and disabled by pathogen effectors. Network buffering could confer this resilience by allowing different parts of the network to compensate for loss of one another’s functions. Networks rich in buffering rely on interactions within the network, but these mechanisms are difficult to study by simple genetic means. Through a network reconstitution strategy, in which we disassemble and stepwise reassemble the plant immune network that mediates Pattern-Triggered-Immunity, we have resolved systems-level regulatory mechanisms underlying the Arabidopsis transcriptome response to the immune stimulant flagellin-22 (flg22). These mechanisms show widespread evidence of interactions among major sub-networks—we call these sectors—in the flg22-responsive transcriptome. Many of these interactions result in network buffering. Resolved regulatory mechanisms show unexpected patterns for how the jasmonate (JA), ethylene (ET), phytoalexin-deficient 4 (PAD4), and salicylate (SA) signaling sectors control the transcriptional response to flg22. We demonstrate that many of the regulatory mechanisms we resolved are not detectable by the traditional genetic approach of single-gene null-mutant analysis. Similar to potential pathogenic perturbations, null-mutant effects on immune signaling can be buffered by the network.
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PLoS Pathogens: Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes (2017)

PLoS Pathogens: Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Plant-parasitic nematodes are destructive pests causing losses of billions of dollars annually. An effective plant defence against pathogens relies on the recognition of pathogen-associated molecular patterns (PAMPs) by surface-localised receptors leading to the activation of PAMP-triggered immunity (PTI). Extensive studies have been conducted to characterise the role of PTI in various models of plant-pathogen interactions. However, far less is known about the role of PTI in roots in general and in plant-nematode interactions in particular. Here we show that nematode-derived proteinaceous elicitor/s is/are capable of inducing PTI in Arabidopsis in a manner dependent on the common immune co-receptor BAK1. Consistent with the role played by BAK1, we identified a leucine-rich repeat receptor-like kinase, termed NILR1 that is specifically regulated upon infection by nematodes. We show that NILR1 is essential for PTI responses initiated by nematodes and nilr1 loss-of-function mutants are hypersusceptible to a broad category of nematodes. To our knowledge, NILR1 is the first example of an immune receptor that is involved in induction of basal immunity (PTI) in plants or in animals in response to nematodes. Manipulation of NILR1 will provide new options for nematode control in crop plants in future.
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Microbiol Mol Biol Rev: Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity (2017)

Microbiol Mol Biol Rev: Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
Fungi and oomycetes are filamentous microorganisms that include a diversity of highly developed pathogens of plants. These are sophisticated modulators of plant processes that secrete an arsenal of effector proteins to target multiple host cell compartments and enable parasitic infection. Genome sequencing revealed complex catalogues of effectors of filamentous pathogens, with some species harboring hundreds of effector genes. Although a large fraction of these effector genes encode secreted proteins with weak or no sequence similarity to known proteins, structural studies have revealed unexpected similarities amid the diversity. This article reviews progress in our understanding of effector structure and function in light of these new insights. We conclude that there is emerging evidence for multiple pathways of evolution of effectors of filamentous plant pathogens but that some families have probably expanded from a common ancestor by duplication and diversification. Conserved folds, such as the oomycete WY and the fungal MAX domains, are not predictive of the precise function of the effectors but serve as a chassis to support protein structural integrity while providing enough plasticity for the effectors to bind different host proteins and evolve unrelated activities inside host cells. Further effector evolution and diversification arise via short linear motifs, domain integration and duplications, and oligomerization.
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BMC Biology: Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thalian...

BMC Biology: Albugo-imposed changes to tryptophan-derived antimicrobial metabolite biosynthesis may contribute to suppression of non-host resistance to Phytophthora infestans in Arabidopsis thalian... | Publications from The Sainsbury Laboratory | Scoop.it
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The Sainsbury Lab's insight:
Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance and enable secondary infection and reproduction of usually non-virulent pathogens, including the potato late blight pathogen Phytophthora infestans on Arabidopsis thaliana. However, the molecular basis of host defense suppression in this complex plant–microbe interaction is unclear. Here, we investigate specific defense mechanisms in Arabidopsis that are suppressed by Albugo infection.
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Nature: Genomic innovation for crop improvement (2017)

Nature: Genomic innovation for crop improvement (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
Crop production needs to increase to secure future food supplies, while reducing its impact on ecosystems. Detailed characterization of plant genomes and genetic diversity is crucial for meeting these challenges. Advances in genome sequencing and assembly are being used to access the large and complex genomes of crops and their wild relatives. These have helped to identify a wide spectrum of genetic variation and permitted the association of genetic diversity with diverse agronomic phenotypes. In combination with improved and automated phenotyping assays and functional genomic studies, genomics is providing new foundations for crop-breeding systems.
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bioRxiv: Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen (2017)

bioRxiv: Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen (2017) | Publications from The Sainsbury Laboratory | Scoop.it

Outbreaks caused by asexual lineages of fungal and oomycete pathogens are an expanding threat to crops, wild animals and natural ecosystems (Fisher et al. 2012, Kupferschmidt 2012). However, the mechanisms underlying genome evolution and phenotypic plasticity in asexual eukaryotic microbes remain poorly understood (Seidl and Thomma 2014). Ever since the 19th century Irish famine, the oomycete Phytophthora infestans has caused recurrent outbreaks on potato and tomato crops that have been primarily caused by the successive rise and migration of pandemic asexual lineages (Cooke et al. 2012, Yoshida et al. 2013, Yoshida et al. 2014). Here, we reveal patterns of genomic and gene expression variation within a P. infestans asexual lineage by compared sibling strains belonging to the South American EC-1 clone that has dominated Andean populations since the 1990s (Forbes et al. 1997, Oyarzun et al. 1998, Delgado et al. 2013, Yoshida et al. 2013, Yoshida et al. 2014). We detected numerous examples of structural variation, nucleotide polymorphisms and gene conversion within the EC-1 clone. Remarkably, 17 genes are not expressed in one of the two EC-1 isolates despite apparent absence of sequence polymorphisms. Among these, silencing of an effector gene was associated with evasion of disease resistance conferred by a potato immune receptor. These results highlight the exceptional genetic and phenotypic plasticity that underpins host adaptation in a pandemic clonal lineage of a eukaryotic plant pathogen.


Via Kamoun Lab @ TSL
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PNAS Commentary: Two-faced TIRs trip the immune switch (2017)

PNAS Commentary: Two-faced TIRs trip the immune switch (2017) | Publications from The Sainsbury Laboratory | Scoop.it
National Academy of Sciences
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Plant Cell Rep: Selection of transformation-efficient barley genotypes based on TFA (transformation amenability) haplotype and higher resolution mapping of the TFA loci (2017)

Plant Cell Rep: Selection of transformation-efficient barley genotypes based on TFA (transformation amenability) haplotype and higher resolution mapping of the TFA loci (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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Barley (Hordeum vulgare) cv. ‘Golden Promise’ is one of the most useful and well-studied cultivars for genetic manipulation. In a previous report, we identified several transformation amenability (TFA) loci responsible for Agrobacterium-mediated transformation using the F2 generation of immature embryos, derived from ‘Haruna Nijo’ × ‘Golden Promise,’ as explants. In this report, we describe higher density mapping of these TFA regions with additional SNP markers using the same transgenic plants. To demonstrate the robustness of transformability alleles at the TFA loci, we genotyped 202 doubled haploid progeny from the cross ‘Golden Promise’ × ‘Full Pint.’ Based on SNP genotype, we selected lines having ‘Golden Promise’ alleles at TFA loci and used them for transformation. Of the successfully transformed lines, DH120366 came the closest to achieving a level of transformation efficiency comparable to ‘Golden Promise.’ The results validate that the genetic substitution of TFA alleles from ‘Golden Promise’ can facilitate the development of transformation-efficient lines from recalcitrant barley cultivars.
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J. Biol. Chem: Autophosphorylation-based calcium (Ca2+) sensitivity priming and Ca2+/Calmodulin inhibition of Arabidopsis thaliana Ca2+-dependent protein kinase 28 (CPK28) (2017)

J. Biol. Chem: Autophosphorylation-based calcium (Ca2+) sensitivity priming and Ca2+/Calmodulin inhibition of Arabidopsis thaliana Ca2+-dependent protein kinase 28 (CPK28) (2017) | Publications from The Sainsbury Laboratory | Scoop.it
The Sainsbury Lab's insight:
Plant calcium (Ca2+) dependent protein kinases (CPKs) represent the primary Ca2+- dependent protein kinase activities in plant systems. CPKs are composed of a dual specificity (Ser/Thr and Tyr) kinase domain tethered to a Calmodulin-like domain (CLD) via an autoinhibitory junction (J). While regulation of CPKs by Ca2+ has been extensively studied, the contribution of autophosphorylation in controlling CPK activity is less well understood. Furthermore, whether Calmodulin (CaM) contributes to CPK regulation, as is the case for Ca2+/CaM-dependent protein kinases (CaMKs) outside the plant lineage, remains an open question. We therefore screened a subset of plant CPKs for CaM-binding and found that CPK28 is a high-affinity Ca2+/CaM-binding protein. Using synthetic peptides and native gel electrophoresis, we coarsely mapped the CaM-binding domain to a site within the CPK28 J domain that overlaps with the known site of intramolecular interaction between the J domain and the CLD. Peptide kinase activity of fully dephosphorylated CPK28 was Ca2+-responsive and was inhibited by Ca2+/CaM. Using in situ autophosphorylated protein, we expand on the known set of CPK28 autophosphorylation sites, and demonstrate that, unexpectedly, autophosphorylated CPK28 had enhanced kinase activity at physiological concentrations of Ca2+ compared with the dephosphorylated protein, suggesting that autophosphorylation functions to prime CPK28 for Ca2+-activation and might also allow CPK28 to remain active when Ca2+ levels are low. Furthermore, CPK28 autophosphorylation substantially reduced sensitivity of the kinase to Ca2+/CaM inhibition. Overall, our analyses uncover new complexities in the control of CPK28 and provide mechanistic support for Ca2+ signaling specificity through Ca2+ sensor priming.
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bioRxiv: Immune receptors with exogenous domain fusions form evolutionary hotspots in grass genomes (2017)

bioRxiv: Immune receptors with exogenous domain fusions form evolutionary hotspots in grass genomes (2017) | Publications from The Sainsbury Laboratory | Scoop.it
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Understanding evolution of plant immunity is necessary to inform rational approaches for genetic control of plant diseases. The plant immune system is innate, encoded in the germline, yet plants are capable of recognizing diverse rapidly evolving pathogens. Plant immune receptors (NLRs) can gain pathogen recognition through point mutation, recombination of recognition domains with other receptors, and through acquisition of novel integrated protein domains. The exact molecular pathways that shape immune repertoire including new domain integration remain unknown. Here, we describe a non-uniform distribution of integrated domains among NLR subfamilies in grasses and identify genomic hotspots that demonstrate rapid expansion of NLR gene fusions. We show that just one clade in the Poaceae is responsible for the majority of unique integration events. Based on these observations we propose a model for the expansion of integrated domain repertoires that involves a flexible NLR acceptor that is capable of fusion to diverse domains derived across the genome. The identification of a subclass of NLRs that is naturally adapted to new domain integration can inform biotechnological approaches for generating synthetic receptors with novel pathogen traps.
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